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Immune stimulation of rainbow trout reveals divergent regulation of MH class II-associated invariant chain isoforms

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Abstract

Major histocompatibility complex (MHC) class II-associated invariant chain is a chaperone responsible for targeting the MHC class II dimer to the endocytic pathway, thus enabling the loading of exogenous antigens onto the MHC class II receptor. In the current study, in vivo and in vitro methods were used to investigate the regulation of the rainbow trout invariant chain proteins S25-7 and INVX, upon immune system activation. Whole rainbow trout and the macrophage/monocyte-like cell line RTS11 were treated with PMA at concentrations shown to induce IL-1β transcripts and homotypic aggregation of RTS11. S25-7 transcript levels remained unchanged in the gill, spleen, and liver and were found to be significantly decreased in head kidney beginning 24 h post-stimulation. Meanwhile, INVX transcript levels remained unchanged in all tissues studied. Both S25-7 and INVX proteins were produced in gill and spleen tissues but their expression was unaffected by immune system stimulation. Surprisingly, neither INVX nor S25-7 protein was detected in the secondary immune organ, the head kidney. Analysis of RTS11 cultures demonstrated that both INVX and S25-7 transcript levels significantly increased at 96 h and 120 h following PMA stimulation before returning to control levels at 168 h. Meanwhile, at the protein level in RTS11, S25-7 remained unchanged while INVX had a significant decrease at 168 h post-stimulation. These results indicate that neither INVX nor S25-7 is upregulated upon immune system activation; thus, teleosts have evolved a system of immune regulation that is different than that found in mammals.

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Acknowledgments

The authors would like to thank Martin Ryan for his technical assistance.

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The work presented in this paper was supported by the Natural Science and Engineering Research Council of Canada grant number 217529 and a Canada Research Chair to BD.

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  1. Department of Biology, University of Waterloo, 200 University Ave W., Waterloo, ON, N2L 3G1, Canada

    Shawna L. Semple, George Heath, Darah Christie, Marsela Braunstein, Stephen C. Kales & Brian Dixon

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Correspondence to Brian Dixon.

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All fish were kept and handled under a permit from the University of Waterloo Animal Care Committee according to CCAC guidelines. All procedures were performed following guidelines of the Animal Care Committee of the University of Waterloo.

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Semple, S.L., Heath, G., Christie, D. et al. Immune stimulation of rainbow trout reveals divergent regulation of MH class II-associated invariant chain isoforms. Immunogenetics 71, 407–420 (2019). https://doi.org/10.1007/s00251-019-01115-y

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